Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons

It is widely believed that information storage in neuronal circuits involves nanoscopic structural changes at synapses, resulting in the formation of synaptic engrams. However, direct evidence for this hypothesis is lacking. To test this conjecture, we combined chemical potentiation, functional anal...

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Published in:PLoS biology Vol. 22; no. 11; p. e3002879
Main Authors: Kim, Olena, Okamoto, Yuji, Kaufmann, Walter A., Brose, Nils, Shigemoto, Ryuichi, Jonas, Peter
Format: Journal Article
Language:English
Published: United States Public Library of Science 18.11.2024
Public Library of Science (PLoS)
Subjects:
Adenosine
Animals
Biology and Life Sciences
Brain research
Calcium channels
Calcium channels (voltage-gated)
Calcium Channels, N-Type - metabolism
Calcium ions
Cerebrospinal fluid
Colforsin - pharmacology
Coupling
Cyclic adenylic acid
Cyclic AMP - metabolism
Cyclic AMP-Dependent Protein Kinases - metabolism
Electron microscopy
Forskolin
Freeze-fracture
Functional analysis
Funding
Health aspects
Hippocampus
Hippocampus (Brain)
Hippocampus - cytology
Hippocampus - metabolism
Hippocampus - physiology
Human information processing
Information storage
Information storage and retrieval
Male
Medicine and Health Sciences
Mice
Microscopy
Mossy Fibers, Hippocampal - metabolism
Mossy Fibers, Hippocampal - physiology
Mossy Fibers, Hippocampal - ultrastructure
Nerve Tissue Proteins - metabolism
Neural circuitry
Neuronal Plasticity - physiology
Physical Sciences
Physiological aspects
Plastic memory
Potentiation
Presynapse
Presynaptic plasticity
Presynaptic Terminals - metabolism
Presynaptic Terminals - physiology
Protein kinase A
Protein kinases
Psychological aspects
Rats
Reconfiguration
Structural analysis
Synapses
Synaptic transmission
Synaptic Transmission - physiology
Synaptic Vesicles - metabolism
Synaptic Vesicles - physiology
Synaptic Vesicles - ultrastructure
Synaptogenesis
Vesicles
Germany
Puerto Rico
ISSN:1545-7885, 1544-9173, 1545-7885
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Abstract It is widely believed that information storage in neuronal circuits involves nanoscopic structural changes at synapses, resulting in the formation of synaptic engrams. However, direct evidence for this hypothesis is lacking. To test this conjecture, we combined chemical potentiation, functional analysis by paired pre-postsynaptic recordings, and structural analysis by electron microscopy (EM) and freeze-fracture replica labeling (FRL) at the rodent hippocampal mossy fiber synapse, a key synapse in the trisynaptic circuit of the hippocampus. Biophysical analysis of synaptic transmission revealed that forskolin-induced chemical potentiation increased the readily releasable vesicle pool size and vesicular release probability by 146% and 49%, respectively. Structural analysis of mossy fiber synapses by EM and FRL demonstrated an increase in the number of vesicles close to the plasma membrane and the number of clusters of the priming protein Munc13-1, indicating an increase in the number of both docked and primed vesicles. Furthermore, FRL analysis revealed a significant reduction of the distance between Munc13-1 and Ca V 2.1 Ca 2+ channels, suggesting reconfiguration of the channel-vesicle coupling nanotopography. Our results indicate that presynaptic plasticity is associated with structural reorganization of active zones. We propose that changes in potential nanoscopic organization at synaptic vesicle release sites may be correlates of learning and memory at a plastic central synapse.
AbstractList It is widely believed that information storage in neuronal circuits involves nanoscopic structural changes at synapses, resulting in the formation of synaptic engrams. However, direct evidence for this hypothesis is lacking. To test this conjecture, we combined chemical potentiation, functional analysis by paired pre-postsynaptic recordings, and structural analysis by electron microscopy (EM) and freeze-fracture replica labeling (FRL) at the rodent hippocampal mossy fiber synapse, a key synapse in the trisynaptic circuit of the hippocampus. Biophysical analysis of synaptic transmission revealed that forskolin-induced chemical potentiation increased the readily releasable vesicle pool size and vesicular release probability by 146% and 49%, respectively. Structural analysis of mossy fiber synapses by EM and FRL demonstrated an increase in the number of vesicles close to the plasma membrane and the number of clusters of the priming protein Munc13-1, indicating an increase in the number of both docked and primed vesicles. Furthermore, FRL analysis revealed a significant reduction of the distance between Munc13-1 and Ca.sub.V 2.1 Ca.sup.2+ channels, suggesting reconfiguration of the channel-vesicle coupling nanotopography. Our results indicate that presynaptic plasticity is associated with structural reorganization of active zones. We propose that changes in potential nanoscopic organization at synaptic vesicle release sites may be correlates of learning and memory at a plastic central synapse.
It is widely believed that information storage in neuronal circuits involves nanoscopic structural changes at synapses, resulting in the formation of synaptic engrams. However, direct evidence for this hypothesis is lacking. To test this conjecture, we combined chemical potentiation, functional analysis by paired pre-postsynaptic recordings, and structural analysis by electron microscopy (EM) and freeze-fracture replica labeling (FRL) at the rodent hippocampal mossy fiber synapse, a key synapse in the trisynaptic circuit of the hippocampus. Biophysical analysis of synaptic transmission revealed that forskolin-induced chemical potentiation increased the readily releasable vesicle pool size and vesicular release probability by 146% and 49%, respectively. Structural analysis of mossy fiber synapses by EM and FRL demonstrated an increase in the number of vesicles close to the plasma membrane and the number of clusters of the priming protein Munc13-1, indicating an increase in the number of both docked and primed vesicles. Furthermore, FRL analysis revealed a significant reduction of the distance between Munc13-1 and CaV2.1 Ca2+ channels, suggesting reconfiguration of the channel-vesicle coupling nanotopography. Our results indicate that presynaptic plasticity is associated with structural reorganization of active zones. We propose that changes in potential nanoscopic organization at synaptic vesicle release sites may be correlates of learning and memory at a plastic central synapse. Information storage in neuronal circuits is hypothesized to involve nanoscopic structural changes at synapses, but direct evidence for this is lacking. This study uses nanophysiology and functional electron microscopy to reveal structural changes of hippocampal active zones during chemical potentiation.
It is widely believed that information storage in neuronal circuits involves nanoscopic structural changes at synapses, resulting in the formation of synaptic engrams. However, direct evidence for this hypothesis is lacking. To test this conjecture, we combined chemical potentiation, functional analysis by paired pre-postsynaptic recordings, and structural analysis by electron microscopy (EM) and freeze-fracture replica labeling (FRL) at the rodent hippocampal mossy fiber synapse, a key synapse in the trisynaptic circuit of the hippocampus. Biophysical analysis of synaptic transmission revealed that forskolin-induced chemical potentiation increased the readily releasable vesicle pool size and vesicular release probability by 146% and 49%, respectively. Structural analysis of mossy fiber synapses by EM and FRL demonstrated an increase in the number of vesicles close to the plasma membrane and the number of clusters of the priming protein Munc13-1, indicating an increase in the number of both docked and primed vesicles. Furthermore, FRL analysis revealed a significant reduction of the distance between Munc13-1 and CaV2.1 Ca2+ channels, suggesting reconfiguration of the channel-vesicle coupling nanotopography. Our results indicate that presynaptic plasticity is associated with structural reorganization of active zones. We propose that changes in potential nanoscopic organization at synaptic vesicle release sites may be correlates of learning and memory at a plastic central synapse.
It is widely believed that information storage in neuronal circuits involves nanoscopic structural changes at synapses, resulting in the formation of synaptic engrams. However, direct evidence for this hypothesis is lacking. To test this conjecture, we combined chemical potentiation, functional analysis by paired pre-postsynaptic recordings, and structural analysis by electron microscopy (EM) and freeze-fracture replica labeling (FRL) at the rodent hippocampal mossy fiber synapse, a key synapse in the trisynaptic circuit of the hippocampus. Biophysical analysis of synaptic transmission revealed that forskolin-induced chemical potentiation increased the readily releasable vesicle pool size and vesicular release probability by 146% and 49%, respectively. Structural analysis of mossy fiber synapses by EM and FRL demonstrated an increase in the number of vesicles close to the plasma membrane and the number of clusters of the priming protein Munc13-1, indicating an increase in the number of both docked and primed vesicles. Furthermore, FRL analysis revealed a significant reduction of the distance between Munc13-1 and Ca V 2.1 Ca 2+ channels, suggesting reconfiguration of the channel-vesicle coupling nanotopography. Our results indicate that presynaptic plasticity is associated with structural reorganization of active zones. We propose that changes in potential nanoscopic organization at synaptic vesicle release sites may be correlates of learning and memory at a plastic central synapse.
It is widely believed that information storage in neuronal circuits involves nanoscopic structural changes at synapses, resulting in the formation of synaptic engrams. However, direct evidence for this hypothesis is lacking. To test this conjecture, we combined chemical potentiation, functional analysis by paired pre-postsynaptic recordings, and structural analysis by electron microscopy (EM) and freeze-fracture replica labeling (FRL) at the rodent hippocampal mossy fiber synapse, a key synapse in the trisynaptic circuit of the hippocampus. Biophysical analysis of synaptic transmission revealed that forskolin-induced chemical potentiation increased the readily releasable vesicle pool size and vesicular release probability by 146% and 49%, respectively. Structural analysis of mossy fiber synapses by EM and FRL demonstrated an increase in the number of vesicles close to the plasma membrane and the number of clusters of the priming protein Munc13-1, indicating an increase in the number of both docked and primed vesicles. Furthermore, FRL analysis revealed a significant reduction of the distance between Munc13-1 and CaV2.1 Ca2+ channels, suggesting reconfiguration of the channel-vesicle coupling nanotopography. Our results indicate that presynaptic plasticity is associated with structural reorganization of active zones. We propose that changes in potential nanoscopic organization at synaptic vesicle release sites may be correlates of learning and memory at a plastic central synapse.It is widely believed that information storage in neuronal circuits involves nanoscopic structural changes at synapses, resulting in the formation of synaptic engrams. However, direct evidence for this hypothesis is lacking. To test this conjecture, we combined chemical potentiation, functional analysis by paired pre-postsynaptic recordings, and structural analysis by electron microscopy (EM) and freeze-fracture replica labeling (FRL) at the rodent hippocampal mossy fiber synapse, a key synapse in the trisynaptic circuit of the hippocampus. Biophysical analysis of synaptic transmission revealed that forskolin-induced chemical potentiation increased the readily releasable vesicle pool size and vesicular release probability by 146% and 49%, respectively. Structural analysis of mossy fiber synapses by EM and FRL demonstrated an increase in the number of vesicles close to the plasma membrane and the number of clusters of the priming protein Munc13-1, indicating an increase in the number of both docked and primed vesicles. Furthermore, FRL analysis revealed a significant reduction of the distance between Munc13-1 and CaV2.1 Ca2+ channels, suggesting reconfiguration of the channel-vesicle coupling nanotopography. Our results indicate that presynaptic plasticity is associated with structural reorganization of active zones. We propose that changes in potential nanoscopic organization at synaptic vesicle release sites may be correlates of learning and memory at a plastic central synapse.
Audience Academic
Author Kim, Olena
Jonas, Peter
Kaufmann, Walter A.
Shigemoto, Ryuichi
Okamoto, Yuji
Brose, Nils
AuthorAffiliation 2 Department of Molecular Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Göttingen, Germany
1 Institute of Science and Technology Austria (ISTA), Klosterneuburg, Austria
Universität Regensburg, GERMANY
AuthorAffiliation_xml – name: Universität Regensburg, GERMANY
– name: 2 Department of Molecular Neurobiology, Max Planck Institute for Multidisciplinary Sciences, Göttingen, Germany
– name: 1 Institute of Science and Technology Austria (ISTA), Klosterneuburg, Austria
Author_xml – sequence: 1
  givenname: Olena
  orcidid: 0000-0003-2344-1039
  surname: Kim
  fullname: Kim, Olena
– sequence: 2
  givenname: Yuji
  orcidid: 0000-0003-0408-6094
  surname: Okamoto
  fullname: Okamoto, Yuji
– sequence: 3
  givenname: Walter A.
  surname: Kaufmann
  fullname: Kaufmann, Walter A.
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  givenname: Nils
  surname: Brose
  fullname: Brose, Nils
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BackLink https://www.ncbi.nlm.nih.gov/pubmed/39556620$$D View this record in MEDLINE/PubMed
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CitedBy_id crossref_primary_10_1038_s41467_025_62420_7
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Copyright Copyright: © 2024 Kim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
COPYRIGHT 2024 Public Library of Science
2024 Kim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
2024 Kim et al 2024 Kim et al
2024 Kim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
Copyright_xml – notice: Copyright: © 2024 Kim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
– notice: COPYRIGHT 2024 Public Library of Science
– notice: 2024 Kim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
– notice: 2024 Kim et al 2024 Kim et al
– notice: 2024 Kim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.
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License Copyright: © 2024 Kim et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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Current address: Institute of Molecular Biotechnology of the Austrian Academy of Science (IMBA), Vienna, Austria
Current address: Department of Cell Physiology, Graduate School of Medicine, Akita University, Akita, Japan
The authors have declared that no competing interests exist.
ORCID 0000-0003-2344-1039
0000-0003-0408-6094
0000-0001-5001-4804
OpenAccessLink http://dx.doi.org/10.1371/journal.pbio.3002879
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SSID ssj0022928
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Snippet It is widely believed that information storage in neuronal circuits involves nanoscopic structural changes at synapses, resulting in the formation of synaptic...
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StartPage e3002879
SubjectTerms Adenosine
Animals
Biology and Life Sciences
Brain research
Calcium channels
Calcium channels (voltage-gated)
Calcium Channels, N-Type - metabolism
Calcium ions
Cerebrospinal fluid
Colforsin - pharmacology
Coupling
Cyclic adenylic acid
Cyclic AMP - metabolism
Cyclic AMP-Dependent Protein Kinases - metabolism
Electron microscopy
Forskolin
Freeze-fracture
Functional analysis
Funding
Health aspects
Hippocampus
Hippocampus (Brain)
Hippocampus - cytology
Hippocampus - metabolism
Hippocampus - physiology
Human information processing
Information storage
Information storage and retrieval
Male
Medicine and Health Sciences
Mice
Microscopy
Mossy Fibers, Hippocampal - metabolism
Mossy Fibers, Hippocampal - physiology
Mossy Fibers, Hippocampal - ultrastructure
Nerve Tissue Proteins - metabolism
Neural circuitry
Neuronal Plasticity - physiology
Physical Sciences
Physiological aspects
Plastic memory
Potentiation
Presynapse
Presynaptic plasticity
Presynaptic Terminals - metabolism
Presynaptic Terminals - physiology
Protein kinase A
Protein kinases
Psychological aspects
Rats
Reconfiguration
Structural analysis
Synapses
Synaptic transmission
Synaptic Transmission - physiology
Synaptic Vesicles - metabolism
Synaptic Vesicles - physiology
Synaptic Vesicles - ultrastructure
Synaptogenesis
Vesicles
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Title Presynaptic cAMP-PKA-mediated potentiation induces reconfiguration of synaptic vesicle pools and channel-vesicle coupling at hippocampal mossy fiber boutons
URI https://www.ncbi.nlm.nih.gov/pubmed/39556620
https://www.proquest.com/docview/3270570140
https://www.proquest.com/docview/3130203265
https://pubmed.ncbi.nlm.nih.gov/PMC11573138
https://doaj.org/article/426c996843b6429ca11a4a0dd736a5cc
http://dx.doi.org/10.1371/journal.pbio.3002879
Volume 22
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